Mesothelial Cells Promote Early Ovarian Cancer Metastasis through Fibronectin Secretion
Open accessAbstract
Ovarian cancer (OvCa) metastasizes to organs in the abdominal cavity, such as the omentum, which are covered by a single layer of mesothelial cells. Mesothelial cells are generally thought to be "bystanders" to the metastatic process and simply displaced by OvCa cells to access the submesothelial extracellular matrix. Here, using organotypic 3D cultures, we found that primary human mesothelial cells secrete fibronectin in the presence of OvCa cells. Moreover, we evaluated the tumor stroma of 108 human omental metastases and determined that fibronectin was consistently overexpressed in these patients. Blocking fibronectin production in primary mesothelial cells in vitro or in murine models, either genetically (fibronectin 1 floxed mouse model) or via siRNA, decreased adhesion, invasion, proliferation, and metastasis of OvCa cells. Using a coculture model, we determined that OvCa cells secrete TGF-β1, which in turn activates a TGF-β receptor/RAC1/SMAD-dependent signaling pathway in the mesothelial cells that promotes a mesenchymal phenotype and transcriptional upregulation of fibronectin. Additionally, blocking α5 or β1 integrin function with antibodies reduced metastasis in an orthotopic preclinical model of OvCa metastasis. These findings indicate that cancer-associated mesothelial cells promote colonization during the initial steps of OvCa metastasis and suggest that mesothelial cells actively contribute to metastasis.
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The organotypic mesothelial model has been adapted for high throughput drug screening of potential inhibitors of adhesion and invasion.
“This model has also been adapted for high throughput drug screening of potential inhibitors of adhesion and invasion.”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Kenny et al., 2014
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Self-citation
- Authors
- Kenny, H. A., Chiang, C.-Y., White, E. A., Schryver, E. M., Habis, M., Romero, I. L., Ladanyi, A., Penicka, C. V., George, J., Matlin, K., Montag, A., Wroblewski, K., Yamada, S. D., Mazar, A. P., Bowtell, D., & Lengyel, E.
- Affiliations
- University of Chicago (US)
- The University of Melbourne (AU)
- Northwestern University (US)
- Corresponding author
- Lengyel, Ernst
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2014-09-09
- Volume
- 124
- Issue
- 10
- Pages
- 4614-4628
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC4191043
- OpenAlex
- W2133056134
- Cited by
- 303
- References
- 72
- Citations by year
- 2026: 15 · 2025: 12 · 2024: 25 · 2023: 35 · 2022: 27 · 2021: 38 · 2020: 31 · 2019: 28 · 2018: 32 · 2017: 22 · 2016: 21 · 2015: 16 · 2014: 1
- FWCI
- 24.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (4r01ca111882-10)
- National Cancer Institute (R01-CA111882)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD000849)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- ovarian cancer, mesothelial cells, metastasis, fibronectin secretion, omental metastasis, TGF-β1, Rac1, Smad signaling, mesenchymal phenotype, alpha5beta1 integrin, integrin alpha5, tumor stroma, extracellular matrix
- MeSH terms
- Animals, Cell Adhesion, Epithelial Cells, Extracellular Matrix, Female, Fibronectins, Humans, Neoplasm Invasiveness, Neoplasm Metastasis, Ovarian Neoplasms, Signal Transduction, Gene Expression Regulation, Neoplastic, Integrins, Coculture Techniques, RNA, Small Interfering, Cell Line, Tumor, Mice, Transforming Growth Factor beta1
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